Low Oxygen Stress During Early Development Influences Regulation of Hypoxia-Response Genes in Farmed Atlantic Salmon (<i>Salmo salar</i>)

Kelly, Tara; Johnsen, Hanne; Burgerhout, Erik; Tveiten, Helge; Thesslund, Tina; Andersen, Øivind; Robinson, Nick

doi:10.1534/g3.120.401459

Cited by 18 publications

(14 citation statements)

References 71 publications

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“…Oxygen levels above 80% are relevant to aquaculture operation and do not affect salmon growth. Eggs from each of the two groups were kept in triplicate tanks (for more details, see Kelly et al, 2020). After 10 months, the fish were PIT-tagged for individual identification and kept at 80-100% DO.…”

Section: Fish: Experimental Procedures and Samplingmentioning

confidence: 99%

“…We report the immune changes induced in early development and manifested over a long period. Recently, our group showed the effects of hypoxia during early life stages on the transcriptome in start feeding larvae of Atlantic salmon (Kelly et al, 2020). This research was performed as a part of a large trial that investigated the programming effects of the environment during early life.…”

Section: Introductionmentioning

confidence: 99%

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Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa

et al. 2021

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Atlantic salmon is characterized with high sensitivity to low dissolved oxygen (DO) levels. Hypoxia can affect diverse biological processes with consequences that can be manifested immediately or with delay. Effects of hypoxia on the immune system and the resistance to a bacterial pathogen were investigated. Two groups were reared at, respectively, normal (NO, 80–100%) and low (LO, 60%) levels of DO over 10 months after which both groups were reared at NO. Smoltification was initiated after 13 months by a winter signal for 6 weeks, followed by constant light for 6 weeks. Samples were collected at the start and end of the constant light period. Expression of 92 immune and stress genes was analyzed in the gill, head kidney, and spleen using a Biomark HD. Most of differentially expressed genes showed higher levels in LO fish compared to NO fish; many immune genes were downregulated during smoltification and these changes were stronger in NO fish. A notable exception was pro-inflammatory genes upregulated in gill of NO fish. Further, salmon were challenged with Moritella viscosa, the causative agent of winter ulcer. Mortality was registered from 5 days post infection (dpi) to the end of trial at 36 dpi. Survival was consistently higher in NO than LO fish, reaching a maximum difference of 18% at 21–23 dpi that reduced to 10% at the end. Analyses with a genome-wide microarray at 36 dpi showed strong responses to the pathogen in gill and spleen. Notable features were the stimulation of eicosanoid metabolism, suggesting an important role of lipid mediators of inflammation, and the downregulation of chemokines. Many immune effectors were activated, including multiple lectins and acute phase proteins, enzymes producing free radicals, and matrix metalloproteinases. The transcriptomic changes induced with a bacterial challenge were similar in NO and LO. After the challenge, interferons a and g and panel of genes of innate antiviral immunity showed higher expression in LO, especially in the gill. The results from the present study suggest that chronic hypoxia in early life stimulated immune genes and attenuated their downregulation associated with smoltification. However, these changes did not improve protection against a bacterial pathogen of major concern in salmon aquaculture.

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Section: Fish: Experimental Procedures and Samplingmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa

et al. 2021

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“…Hypoxia can increase the expression of HIF-1α in organisms has been confirmed in a large number of studies (Kelly et al, 2020;Wang M. et al, 2021;Xu et al, 2021). HIF-1 is a heterodimer composed of HIF-1α and HIF-1β (Semenza, 1998).…”

Section: Discussionmentioning

confidence: 84%

Effects of Microplastics on Immune Responses of the Yellow Catfish Pelteobagrus fulvidraco Under Hypoxia

Jiang

et al. 2021

Front. Physiol.

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Compared with marine organisms, research on microplastics (MPs) in freshwater organisms is still less although MPs have been widely found in the freshwater ecosystem. Hypoxia is a ubiquitous issue in freshwater aquaculture, and under such scenarios, the toxic effects of MPs on typical aquaculture fish need to be clarified. In this study, we studied the effects of MPs (polystyrene) on specific growth rate (SGR), hypoxia-inducible factor-1α (HIF-1α), tumor necrosis factor-α (TNF-α), interleukin-8 (IL-8), and interferon (IFN) in the yellow catfish (Pelteobagrus fulvidraco) under hypoxic conditions. After 15 days of exposure, the SGR was not affected by MPs or hypoxia. MPs significantly increased the expressions of HIF-1α and TNF-α but inhibited the expression of IFN at high concentration MPs under normoxia. However, hypoxia significantly inhibited the expression of IL-8 and TNF-α under high MP concentration and low MP concentration, respectively. In addition, MPs had significant concentration-dependent inhibitory effects on IFN under hypoxia. Surprisingly, a positive correction between HIF-1α and TNF-α was found in fish. Although hypoxia might alleviate the effects of MPs with low concentrations, the interaction of hypoxia and MPs aggravated the negative effects of MPs on immune factors at high concentration MPs. This study provided new insight into the complex effects of hypoxia and MPs on aquatic organisms, and future studies should focus on the cellular pathways of immune cells in fish. Given that MPs could induce the immune response in fish, considerations should be paid to the impacts of MPs on freshwater aquaculture, and hypoxia should be taken into consideration when evaluating the effects of MPs.

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“…Dissolved oxygen plays an important role in maintaining biochemical and physiological processes. Hypoxia may limit energy processes and adversely affect growth, reproduction, and survival ( Kelly et al 2020 ). Many factors affect the growth and survival of fish; therefore, it is necessary to clarify the mechanism of heat stress responses of smelt to reduce their mortality effectively.…”

Section: Introductionmentioning

confidence: 99%

Draft genome of the Korean smelt Hypomesus nipponensis and its transcriptomic responses to heat stress in the liver and muscle

Xuan

Park

Choi

et al. 2021

G3 Genes|Genomes|Genetics

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Pond smelt (Hypomesus nipponensis) is a cold-freshwater fish species as a winter economic resource of aquaculture in South Korea. Due to its high susceptibility to abnormal water temperature from global warming, a large number of smelt die in hot summer. Here, we present the first draft genome of H. nipponensis and transcriptomic changes in molecular mechanisms or intracellular responses under heat stress. We combined Illumina and PacBio sequencing technologies to generate the draft genome of H. nipponensis. Based on the reference genome, we conducted transcriptome analysis of liver and muscle tissues under normal (NT, 5 °C) versus warm (HT, 23 °C) conditions, to identify heat stress-induced genes and gene categories. We observed a total of 1,987 contigs, with N50 of 0.46 Mbp with a largest contig (3.03 Mbp) in the assembled genome. A total number of 20,644 protein coding genes were predicted, and 19,224 genes were functionally annotated: 15,955 genes for Gene Ontology (GO) terms; and 11,560 genes for KEGG Orthology (KO). We conducted the lost and gained genes analysis compared with three species that human, zebrafish and salmon. In the lost genes analysis, we detected smelt lost 4,461 (22.16%), 2,825 (10.62%), and 1,499 (3.09%) genes compare with above three species, respectively. In the gained genes analysis, we observed smelt gain 1,133 (5.49%), 1,670 (8.09%), and 229 (1.11%) genes compare with above species, respectively. From transcriptome analysis, a total of 297 and 331 differentially expressed genes (DEGs) with False discovery rate (FDR) < 0.05 were identified in the liver and muscle tissues, respectively. Gene enrichment analysis of DEGs indicates that up-regulated genes were significantly enriched for lipid biosynthetic process (GO : 0008610, P < 0.001) and regulation of apoptotic process (GO : 0042981, P < 0.01), and down-regulated genes by immune responses such as myeloid cell differentiation (GO : 0030099, P < 0.001) in the liver under heat stress. In muscle tissue, up-regulated genes were enriched for hypoxia (GO : 0001666, P < 0.05), transcription regulator activity (GO : 0140110, P < 0.001) and calcium-release channel activity (GO : 0015278, P < 0.01), and down-regulated genes for nicotinamide nucleotide biosynthetic process (GO : 0019359, P < 0.01). The results of KEGG pathway analysis were similar to that of gene enrichment analysis. The draft genome and transcriptomic of H. nipponensis will be used as a useful genetic resource for functional and evolutionary studies. Our findings will improve understanding of the molecular mechanisms and heat responses and will be useful for predicting survival of the smelt and its closely related species under global warming.

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Low Oxygen Stress During Early Development Influences Regulation of Hypoxia-Response Genes in Farmed Atlantic Salmon (Salmo salar)

Cited by 18 publications

References 71 publications

Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa

Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa

Effects of Microplastics on Immune Responses of the Yellow Catfish Pelteobagrus fulvidraco Under Hypoxia

Draft genome of the Korean smelt Hypomesus nipponensis and its transcriptomic responses to heat stress in the liver and muscle

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